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Oxidative ATP synthesis in human quadriceps declines during 4 minutes of maximal contractions
Author(s) -
Bartlett Miles F.,
Fitzgerald Liam F.,
Nagarajan Rajakumar,
Hiroi Yeun,
Kent Jane A.
Publication year - 2020
Publication title -
the journal of physiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.802
H-Index - 240
eISSN - 1469-7793
pISSN - 0022-3751
DOI - 10.1113/jp279339
Subject(s) - oxidative phosphorylation , skeletal muscle , glycolysis , atp synthase , adenosine triphosphate , phosphocreatine , bioenergetics , chemistry , oxygen , mitochondrion , metabolism , medicine , biochemistry , endocrinology , biology , energy metabolism , enzyme , organic chemistry
Key points During maximal exercise, skeletal muscle metabolism and oxygen consumption remain elevated despite precipitous declines in power. Presently, it is unclear whether these responses are caused by an increased ATP cost of force generation (ATP COST ) or mitochondrial uncoupling; a process that reduces the efficiency of oxidative ATP synthesis (ATP OX ). To address this gap, we used 31‐phosphorus magnetic resonance spectroscopy to measure changes in ATP COST and ATP OX in human quadriceps during repeated trials of maximal intensity knee extensions lasting up to 4 min. ATP COST remained unchanged. In contrast, ATP OX plateaued by ∼2 min and then declined (∼15%) over the final 2 min. The maximal capacity for ATP OX (V max ), as well as ADP‐specific rates of ATP OX , were also significantly diminished. Collectively, these results suggest that mitochondrial uncoupling, and not increased ATP COST , is responsible for altering the regulation of skeletal muscle metabolism and oxygen consumption during maximal exercise.Abstract The relationship between skeletal muscle oxygen consumption and power output is augmented during exercise at workloads above the lactate threshold. Potential mechanisms for this response have been hypothesized, including increased ATP cost of force generation (ATP COST ) and mitochondrial uncoupling, a process that reduces the efficiency of oxidative ATP synthesis (ATP OX ). To test these hypotheses, we used phosphorus magnetic resonance spectroscopy to non‐invasively measure changes in phosphate concentrations and pH in the vastus lateralis muscle of nine young adults during repeated trials of maximal, all‐out dynamic knee extensions (120°s −1 , 1 every 2 s) lasting 24, 60, 120, and 240 s. ATP OX was measured at each time point from the initial velocity of PCr resynthesis, and ATP COST was calculated as the sum of ATP synthesized by the creatine and adenylate kinase reactions, non‐oxidative glycolysis, ATP OX and net changes in [ATP]. Power output declined in a reproducible manner for all four trials. ATP COST did not change over time (main effect P = 0.45). ATP OX plateaued from 60 to 120 s and then decreased over the final 120 s (main effect P = 0.001). The maximal capacity for oxidative ATP synthesis (V max ), as well as ADP‐specific rates of ATP OX , also decreased over time (main effect P = 0.001, both). Collectively, these results demonstrate that prolonged maximal contraction protocols impair oxidative energetics and implicate mitochondrial uncoupling as the mechanism for this response. The causes of mitochondrial uncoupling are presently unknown but may offer a potential explanation for the dissociation between skeletal muscle power output and oxygen consumption during maximal, all‐out exercise protocols.